Photosynthesis Research

, Volume 114, Issue 2, pp 69–96 | Cite as

Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker

  • Hazem M. Kalaji
  • Vasilij Goltsev
  • Karolina Bosa
  • Suleyman I. Allakhverdiev
  • Reto J. Strasser
  • Govindjee
Review

Abstract

This review is dedicated to David Walker (1928–2012), a pioneer in the field of photosynthesis and chlorophyll fluorescence. We begin this review by presenting the history of light emission studies, from the ancient times. Light emission from plants is of several kinds: prompt fluorescence (PF), delayed fluorescence (DF), thermoluminescence, and phosphorescence. In this article, we focus on PF and DF. Chlorophyll a fluorescence measurements have been used for more than 80 years to study photosynthesis, particularly photosystem II (PSII) since 1961. This technique has become a regular trusted probe in agricultural and biological research. Many measured and calculated parameters are good biomarkers or indicators of plant tolerance to different abiotic and biotic stressors. This would never have been possible without the rapid development of new fluorometers. To date, most of these instruments are based mainly on two different operational principles for measuring variable chlorophyll a fluorescence: (1) a PF signal produced following a pulse-amplitude-modulated excitation and (2) a PF signal emitted during a strong continuous actinic excitation. In addition to fluorometers, other instruments have been developed to measure additional signals, such as DF, originating from PSII, and light-induced absorbance changes due to the photooxidation of P700, from PSI, measured as the absorption decrease (photobleaching) at about 705 nm, or increase at 820 nm. In this review, the technical and theoretical basis of newly developed instruments, allowing for simultaneous measurement of the PF and the DF as well as other parameters is discussed. Special emphasis has been given to a description of comparative measurements on PF and DF. However, DF has been discussed in greater details, since it is much less used and less known than PF, but has a great potential to provide useful qualitative new information on the back reactions of PSII electron transfer. A review concerning the history of fluorometers is also presented.

Keywords

Delayed fluorescence Fluorometers Photosystem II Prompt fluorescence 

References

  1. Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B 104:1–8PubMedCrossRefGoogle Scholar
  2. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32PubMedCrossRefGoogle Scholar
  3. Allakhverdiev SI, Klimov VV, Carpentier R (1994) Variable thermal emission and chlorophyll fluorescence in photosystem II particles. Proc Natl Acad Sci USA 491:281–285CrossRefGoogle Scholar
  4. Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007a) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371PubMedCrossRefGoogle Scholar
  5. Allakhverdiev SI, Shuvalov VA, Klimov VV (2007b) Structure and function of photosystems. Biochim Biophys Acta 176:401–882Google Scholar
  6. Amesz J, Van Gorkom HJ (1978) Delayed fluorescence in photosynthesis. Annu Rev Plant Physiol 29:47–66CrossRefGoogle Scholar
  7. Ananyev G, Dismukes GC (2005) How fast can photosystem II split water? Kinetic performance at high and low frequencies. Photosynth Res 84:355–365PubMedCrossRefGoogle Scholar
  8. Ananyev G, Kolber ZS, Klimov D, Falkowski PG, Berry J, Rascher U, Martin R, Osmond B (2005) Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient device. Glob Change Biol 11:1195–1206CrossRefGoogle Scholar
  9. Antal TK, Krendeleva TE, Rubin AB (2007) Study of photosystem 2 heterogeneity in the sulfur-deficient green alga Chlamydomonas reinhardtii. Photosynth Res 94:13–22PubMedCrossRefGoogle Scholar
  10. Antal TK, Matorin DN, Ilyash LV, Volgusheva AA, Osipov A, Konyuhow IV, Krendeleva TE, Rubin AB (2009) Probing of photosynthetic reactions in four phytoplanktonic algae with a PEA fluorometer. Photosynth Res 102:67–76PubMedCrossRefGoogle Scholar
  11. Arnold W (1965) An electron–hole picture of photosynthesis. J Phys Chem 69:788–791PubMedCrossRefGoogle Scholar
  12. Arnold W (1977) Delayed light in photosynthesis. Annu Rev Biophys Bioeng 6:1–6PubMedCrossRefGoogle Scholar
  13. Arnold W, Davidson JB (1954) The identity of the fluorescent and delayed light emission spectra in Chlorella. J Gen Physiol 36:311–318Google Scholar
  14. Arnold W, Thompson JJ (1956) Delayed light production by blue-green algae, red algae and purple bacteria. J Gen Physiol 36:311–318CrossRefGoogle Scholar
  15. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  16. Askenasy E (1867) Beitrage zur Kenntniss des Chlorophylls und einiger dasselbe begleitender Farbstoffe 11. Bot Zeitung 25:233–238Google Scholar
  17. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113PubMedCrossRefGoogle Scholar
  18. Baker NR, Oxborough K (2000) Carotenoids and antioxidants protect leaves from light. The Biochemist 22:19–24Google Scholar
  19. Baker NR, Oxborough K (2004) Chlorophyll a fluorescence as a probe of photosynthetic productivity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a probe of photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 65–82CrossRefGoogle Scholar
  20. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621PubMedCrossRefGoogle Scholar
  21. Bannister TT, Rice G (1968) Parallel time courses of oxygen evolution and chlorophyll fluorescence. Biochim Biophys Acta 162:555–580PubMedCrossRefGoogle Scholar
  22. Barber J (2002) P680: what is it and where is it? Bioelectrochemistry 55:135–138PubMedCrossRefGoogle Scholar
  23. Barber J, Neumann J (1974) An energy-conservation site between H2O and DBMIB: evidence from msec delayed light and chlorophyll fluorescence studies in chloroplasts. FEBS Lett 40:186–189CrossRefGoogle Scholar
  24. Beard JB (2002) Turf management for golf courses, 2nd edn. Wiley, HobokenGoogle Scholar
  25. Bennoun P, Béal D (1997) Screening algal mutant colonies with altered thylakoid electrochemical gradient through fluorescence and delayed luminescence digital imaging. Photosynth Res 51:161–165CrossRefGoogle Scholar
  26. Berden-Zrimec M, Drinovec L, Molinari I, Zrimec A, Umani SF (2008) Delayed fluorescence as a measure of nutrient limitation in Dunaliellatertiolecta. J Photochem Photobiol B 92:13–18PubMedCrossRefGoogle Scholar
  27. Bertsch WF, Azzi JR (1965) A relative maximum in the decay of long-term delayed light emission from the photosynthetic apparatus. Biochim Biophys Acta 94(1):15–26PubMedCrossRefGoogle Scholar
  28. Bertsch WF, Azzi JR, Davidson JB (1967) Delayed light studies on photosynthetic energy conversion. 1. Identification of the oxygen evolving photoreaction as the delayed light emitter in mutants of Scenedesmus obliquus. Biochim Biophys Acta 143:129–143PubMedCrossRefGoogle Scholar
  29. Bertsch WF, West J, Hill R (1969) Delayed light studies on photosynthetic energy conversion II. Effect of electron acceptors and phosphorylation cofactors on the millisecond emission from chloroplasts. Biochim Biophys Acta 172(3):525–538PubMedCrossRefGoogle Scholar
  30. Bowman R, Caulfield P, Udenfriend S (1955) Spectrophotofluorometric assay throughout the ultraviolet and visible range. Science 122:32–33PubMedCrossRefGoogle Scholar
  31. Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystem I and II. Biochim Biophys Acta 635:542–551PubMedCrossRefGoogle Scholar
  32. Brestič M, Olšovská K, Pivková J (2010) Bioindication of thermotolerance of winter wheat (Triticum aestivum L.) photosynthetic apparatus. Acta Fytotechnica et Zootechnica 13(3):67–71Google Scholar
  33. Brestič M, Zivcak M, Kalaji MH, Carpentier R, Allakhverdiev SI (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem. doi:10.1016/j.plaphy.2012.05.012
  34. Brewster D (1834) On the colours of natural bodies. Trans R Soc Edinb 12:538–545Google Scholar
  35. Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitive study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138PubMedCrossRefGoogle Scholar
  36. Brody SS (1957) Instrument to measure fluorescence lifetimes in the millimicrosecond region. Rev Sci Instrum 28:1021–1026CrossRefGoogle Scholar
  37. Brody SS (2005) Fluorescence lifetime, yield, energy transfer and spectrum in photosynthesis, 1950–1960. In: Govindjee, Beatty JT, Gest H, Allen JF (eds) Discoveries in photosynthesis. Advances in photosynthesis and respiration, vol 20. Springer, Dordrecht, pp 165–170Google Scholar
  38. Brzóstowicz A (2003) Luminescencyjna metoda oceny mrozoodporności roślin [in Polish]. Acta Agrophys 93:5–10Google Scholar
  39. Brzóstowicz A, Murkowski A, Mila A (2003) Luminometr do badania wpływu obniżania temperatury na opóźnioną luminescencję obiektów roślinnych [in Polish]. Acta Agrophys 93:45–57Google Scholar
  40. Buchta J, Grabolle M, Dau H (2007) Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements—method, rationale, and results on the activation energy of dioxygen formation. Biochim Biophys Acta 1767:565–574PubMedCrossRefGoogle Scholar
  41. Buchta J, Shutova T, Samuelsson G, Dau H (2008) Time-resolved delayed chlorophyll fluorescence to study the influence of bicarbonate on a green algae mutant photosystem II. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 35–38CrossRefGoogle Scholar
  42. Bukhov NG, Carpentier R (2000) Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiol Plant 110:279–285CrossRefGoogle Scholar
  43. Bukhov NG, Carpentier R (2003) Measurement of photochemical quenching of absorbed quanta in photosystem I of intact leaves using simultaneous measurements of absorbance changes at 830 nm and thermal dissipation. Planta 216:630–638PubMedGoogle Scholar
  44. Bukhov NG, Carpentier R, Samson G (2001) Heterogeneity of photosystem I reaction centers in barley leaves as related to the donation from stromal reductants. Photosynth Res 70:273–279PubMedCrossRefGoogle Scholar
  45. Bussotti F (2004) Assessment of stress conditions in Quercus ilex L. leaves by O–J–I–P chlorophyll a fluorescence analysis. Plant Biosyst 13:101–109CrossRefGoogle Scholar
  46. Bussotti F, Agati G, Desotgiu R, Matteini P, Tani C (2005) Ozone foliar symptoms in woody plants assessed with ultrastructural and fluorescence analysis. New Phytol 166:941–955PubMedCrossRefGoogle Scholar
  47. Bussotti F, Pollastrini M, Cascio C, Desotgiu R, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Pellegrini E, Carucci MG, Salvatori E, Fusaro L, Piccotto M, Malaspina P, Manfredi A, Roccotello E, Toscano S, Gottardini E, Cristofori A, Fini A, Weber D, Baldassarre V, Barbanti L, Monti A, Strasser RJ (2011a) Conclusive remarks. Reliability and comparability of chlorophyll fluorescence data from several field teams. Environ Exp Bot 73:116–119CrossRefGoogle Scholar
  48. Bussotti F, Desotgiu R, Cascio C, Pollastrini M, Gravano E, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Salvatori E, Manes F, Schaub M, Strasser RJ (2011b) Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ Exp Bot 73:19–30CrossRefGoogle Scholar
  49. Butler WL (1966) Fluorescence yield in photosynthetic systems and its relation to electron transport. In: Sanadi DR (ed) Current topics in bioenergetics. Academic Press, New York, pp 49–73Google Scholar
  50. Butler WL, Strasser RJ (1977) Tripartite model for the photochemical apparatus of green plant photosynthesis. Proc Natl Acad Sci USA 74:3382–3385PubMedCrossRefGoogle Scholar
  51. Cario G, Franck J (1922) Über Zerlegugen von Wasserstoffmolekülen durch aggregate Quecksilberatome. Z Physik 11:161–166CrossRefGoogle Scholar
  52. Carter AG, Knapp AK (2001) Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. Am J Bot 88:677–684PubMedCrossRefGoogle Scholar
  53. Christen G, Reifarth F, Renger G (1998) On the origin of the ‘35-ms kinetics’ of P680+ reduction in photosystem II with an intact water oxidising complex. FEBS Lett 429:49–52PubMedCrossRefGoogle Scholar
  54. Christen G, Steffen R, Renger G (2000) Delayed fluorescence emitted from light harvesting complex II and photosystem II of higher plants in the 100 ns–5 μs time domain. FEBS Lett 475:103–106PubMedCrossRefGoogle Scholar
  55. Clayton RK (1969) Characteristics of prompt and delayed fluorescence from spinach chloroplasts. Biophys J 9:60–76PubMedCrossRefGoogle Scholar
  56. Clayton RK (1971) Light and living matter, vols 1, 2. McGraw Hill, New YorkGoogle Scholar
  57. Clegg RM, Sener M, Govindjee (2010) From Förster resonance energy transfer (FRET) to coherent resonance energy transfer (CRET) and back—A wheens o’ mickles mak’s a muckle. SPIE Proceedings. In: Alfano RR (ed) Optical biopsy. Proceedings of SPIE, vol VII, SPIE, Bellingham, WA, pp 7561–7572 (CID number: 3509 75610C, 2010, pp 1–21)Google Scholar
  58. Crofts AR, Wraight CA, Fleischman DE (1971) Energy conservation in the photochemical reactions of photosynthesis and its relation to delayed fluorescence. FEBS Lett 15:89–100PubMedCrossRefGoogle Scholar
  59. Dau H, Sauer K (1996) Exciton equilibration and photosystem II exciton dynamics—a fluorescence study on photosystem II membrane particles of spinach. Biochim Biophys Acta 1273:175–190CrossRefGoogle Scholar
  60. Dau H, Zaharieva I (2009) Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation. Accounts Chem Res 42:1861–1870CrossRefGoogle Scholar
  61. Dau H, Zaharieva I, Haumann M (2012) Recent developments in research on water oxidation by photosystem II. Cur Opin Chem Biol 16:1–8CrossRefGoogle Scholar
  62. Delieu TJ, Walker DA (1983) Simultaneous measurement of oxygen evolution and chlorophyll fluorescence from leaf pieces. Plant Physiol 73:534–541PubMedCrossRefGoogle Scholar
  63. Dell’Aquila AR, Van der Schoor R, Jalink H (2002) Application of chlorophyll fluorescence in sorting controlled deteriorated white cabbage (Brassica oleracea L.) seeds. Seed Sci Technol 30:689–695Google Scholar
  64. Delosme R, Joliot P, Lavorel J (1959) Sur la complémentarité de la fluorescence et de l’émission d’oxygène pendant la periode d’induction de la photosynthèse. C R Acad Sci Paris 249:1409–1411Google Scholar
  65. Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plantarum 98:254–264Google Scholar
  66. Demmig-Adams B, Adams WW III, Mattoo AK (eds) (2005) Photoprotection, photoinhibition, gene regulation, and environment. Advances in photosynthesis and respiration, vol 21. Springer, Dordrecht (paperback: 2008)Google Scholar
  67. Dietz KJ, Schreiber U, Heber U (1985) The relationship between the redox state of QA and photosynthesis in leaves at various carbon dioxide, oxygen, and light regimes. Planta 166:219–226CrossRefGoogle Scholar
  68. Dmitrievsky OD, Ermolaev VL, Terrenin AN (1957) The fluorescence lifetime of chlorophyll a in Chlorella cells. Proc USSR Acad Sci 114:75–78Google Scholar
  69. Ducruet JM, Peeva V, Havaux M (2007) Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynth Res 93:159–171PubMedCrossRefGoogle Scholar
  70. Durrant JR, Klug DR, Kwa SLS, van Grondelle R, Porter G, Dekker JP (1995) A multimer model for P680, the primary electron donor of photosystem II. Proc Natl Acad Sci USA 92:4798–4802PubMedCrossRefGoogle Scholar
  71. Duysens LNM (1952) Transfer of excitation energy in photosynthesis. State University, Utrecht, The Netherlands, Doctoral ThesisGoogle Scholar
  72. Duysens LNM, Amesz J (1957) Fluorescence spectrometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region. Biochim Biophys Acta 24:19–26PubMedCrossRefGoogle Scholar
  73. Duysens LNM, Sweers HE (1963) Mechanism of two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists (ed) Studies on microalgae and photosynthetic bacteria. University of Tokyo Press, Tokyo, pp 353–372Google Scholar
  74. Eaton-Rye JJ, Govindjee (1988a) Electron transfer through the quinone acceptor complex of photosystem II in bicarbonate-depleted spinach thylakoid membranes as a function of actinic flash number and frequency. Biochim Biophys Acta 935:237–247CrossRefGoogle Scholar
  75. Eaton-Rye JJ, Govindjee (1988b) Electron transfer through the quinone acceptor complex of photosystem II after one or two actinic flashes in bicarbonate-depleted spinach thylakoid membranes. Biochim Biophys Acta 935:248–257CrossRefGoogle Scholar
  76. Edwards GE, Heber U (2012) David Alan Walker (1928–2012). Photosynth Res 112:91–102PubMedCrossRefGoogle Scholar
  77. Emerson R, Chalmers RV, Cederstrand CN (1957) Some factors influencing the long wave limit of photosynthesis. Proc Natl Acad Sci USA 43:133–143PubMedCrossRefGoogle Scholar
  78. Evans EH, Crofts AT (1973) The relationship between delayed fluorescence and the H+ gradient in chloroplasts. Biochim Biophys Acta 292:130–139PubMedCrossRefGoogle Scholar
  79. Fleischman DE, Mayne BC (1973) Chemically and physically induced luminescence as a probe of photosynthetic mechanism. Curr Topics Bioeng 5:77–105Google Scholar
  80. Flexas J, Briantais JM, Cerovic Z, Medrano H, Moya I (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sens Environ 73:283–297CrossRefGoogle Scholar
  81. Gaevsky NA, Morgun VN (1993) Use of variable fluorescence and delayed light emission to studies of plant physiology. Plant Physiol (Moscow) 40:136–145Google Scholar
  82. Gaevsky NA, Gehman AV, Goltsev V (1992) Device for fluorescence diagnostics of state of water ecosystems. In: Proceedings of VI national conference of biomedical and physical engineering, Sofia, pp 110–118 (in Bulgarian)Google Scholar
  83. Garcia-Mendoza E, Ocampo-Alvarez H, Govindjee (2011) Photoprotection in the brown alga Macrocystis pyrifera: evolutionary implications. J Photochem Photobiol B 104:377–385PubMedCrossRefGoogle Scholar
  84. Gasanov RA, Govindjee (1974) Chlorophyll fluorescence characteristics of photosystem I and II from grana and photosystem I from stroma lamellae. Z Pflanzenphysiol 72:193–202Google Scholar
  85. Goltsev V, Yordanov I (1997) Mathematical model of prompt and delayed chlorophyll fluorescence induction kinetics. Photosynthetica 33:571–586Google Scholar
  86. Goltsev V, Ortoidze TV, Sokolov ZN, Matorin DN, Venediktov PS (1980) Delayed luminescence yield kinetics in flash illuminated green plants. Plant Sci Lett 19:339–346CrossRefGoogle Scholar
  87. Goltsev V, Traikov L, Hristov V (1998) Effects of exogenous electron acceptors on kinetic characteristics of prompt and delayed fluorescence in atrazine inhibited thylakoid membranes. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic, Dordrecht, pp 3885–3888Google Scholar
  88. Goltsev V, Zaharieva I, Lambrev P, Yordanov I, Strasser RJ (2003) Simultaneous analysis of prompt and delayed chlorophyll a fluorescence in leaves during the induction period of dark to light adaptation. J Theor Biol 225:171–183PubMedCrossRefGoogle Scholar
  89. Goltsev V, Chernev P, Zaharieva I, Lambrev P, Strasser RJ (2005) Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range. Photosynth Res 84:209–215PubMedCrossRefGoogle Scholar
  90. Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed fluorescence in photosynthesis. Photosynth Res 101:217–232PubMedCrossRefGoogle Scholar
  91. Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji MH, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490–1498PubMedCrossRefGoogle Scholar
  92. Gorbunov MY, Kolber ZS, Falkowski PG (1999) Measuring photosynthetic parameters in individual algal cells by fast repetition rate fluorometry. Photosynth Res 62:141–153CrossRefGoogle Scholar
  93. Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160CrossRefGoogle Scholar
  94. Govindjee (2004) Chlorophyll a fluorescence: a bit of basics and history. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a probe of photosynthesis. Kluwer Academic, Dordrecht, pp 1–42CrossRefGoogle Scholar
  95. Govindjee, Jursinic P (1979) Photosynthesis and fast changes in light emission by green plants. Photochem Photobiol Rev 4:125–205CrossRefGoogle Scholar
  96. Govindjee, Papageorgiou GC (1971) Chlorophyll fluorescence and photosynthesis: fluorescence transients. In: Giese AC (ed) Photophysiology. Academic Press, New York, pp 1–46Google Scholar
  97. Govindjee, Yoo H (2007) The International Society of Photosynthesis Research (ISPR) and its associated International Congress on Photosynthesis (ICP): a pictorial report. Photosynth Res 91:95–106CrossRefGoogle Scholar
  98. Govindjee, Ichimura S, Cederstrand C, Rabinowitch E (1960) Effect of combining far-red light with shorter wavelight in the excitation of fluorescence in Chlorella. Arch Biochem Biophys 89:322–323PubMedCrossRefGoogle Scholar
  99. Govindjee, Pulles MPJ, Govindjee R, Van Gorkom HM, Duysens LNM (1976) Inhibition of the reoxidation of the secondary electron acceptor of photosystem II by bicarbonate depletion. Biochim Biophys Acta 449:602–605PubMedCrossRefGoogle Scholar
  100. Govindjee, Amesz J, Fork DC (eds) (1986) Light emission by plants and bacteria. Academic Press, OrlandoGoogle Scholar
  101. Govindjee, Kern JF, Messinger J, Whitmarsh J (2010) Photosystem II, encyclopedia of life sciences. Wiley, Chichester. doi:10.1002/9780470015902.a0000669.pub2
  102. Grabolle M, Dau H (2005) Energetics of primary and secondary electron transfer in photosystem II membrane particles of spinach revisited on basis of recombination-fluorescence measurements. Biochim Biophys Acta 1708:209–218PubMedCrossRefGoogle Scholar
  103. Grace J, Nichol C, Disney M, Lewis P, Quaife T, Bowyer P (2007) Can we measure terrestrial photosynthesis from space directly, using spectral reflectance and fluorescence? Glob Change Biol 13:1484–1497CrossRefGoogle Scholar
  104. Gururani MA, Upadhyaya CP, Strasser RJ, Woong YJ, Park SW (2012) Physiological and biochemical responses of transgenic potato plants with altered expression of PSII manganese stabilizing protein. Plant Phys Biochem 58C:182–194CrossRefGoogle Scholar
  105. Harbinson J, Hedley CL (1993) Changes in P-700 oxidation during the early stages of the induction of photosynthesis. Plant Physiol 103:660–694Google Scholar
  106. Harvey EN (1957) A history of luminescence from the earliest times until 1900. American Philosophical Society, Library of Congress Card #: 57-8126; J. H. FURST Company, Baltimore, Maryland, USAGoogle Scholar
  107. Haug A, Jaquet DD, Beall HC (1972) Light emission from the Scenedesmus obliquus wild type, mutant 8, and mutant 11 strains measured under steady-state conditions between 4 nanoseconds and 10 seconds. Biochim Biophys Acta 283:92–99PubMedCrossRefGoogle Scholar
  108. Henriques F (2009) Leaf chlorophyll fluorescence: background and fundamentals for plant biologists. Bot Rev 75:249–270CrossRefGoogle Scholar
  109. Hideg E, Kobayashi M, Inaba H (1990) Ultra weak photoemission from dark-adapted leaves and isolated chloroplasts. FEBS Lett 275:121–124PubMedCrossRefGoogle Scholar
  110. Hideg E, Kobayashi M, Inaba H (1991) The far red induced slow component of delayed light from chloroplasts is emitted from photosystem-II-evidence from emission-spectroscopy. Photosynth Res 29:107–112CrossRefGoogle Scholar
  111. Hipkins MF, Barber J (1974) Estimation of the activation energy for millisecond delayed fluorescence from uncoupled chloroplasts. FEBS Lett 42:289–292PubMedCrossRefGoogle Scholar
  112. Hodak J, Martini I, Hartland GV (1998) Spectroscopy and dynamics of nanometersized noble metal particles. J Phys Chem B 102:6958CrossRefGoogle Scholar
  113. Holzwarth AR, Müller MG, Reus M, Nowaczyk M, Sander J, Rögner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA 103:6895–6900PubMedCrossRefGoogle Scholar
  114. Horton P (1983) Relationships between electron transfer and carbon assimilation; simultaneous measurement of chlorophyll fluorescence transthylakoid pH gradient and O2 evolution in isolated chloroplasts. Proc R Soc Lond Ser B 217:405–416CrossRefGoogle Scholar
  115. Itoh S, Murata N (1973) Correlation between delayed light emission and fluorescence of chlorophyll a in system II particles derived from spinach chloroplasts. Photochem Photobiol 18:209–218CrossRefGoogle Scholar
  116. Itoh S, Murata N, Takamiya A (1971) Studies on the delayed light emission in spinach chloroplasts. I. Nature of two phases in development of the millisecond delayed light emission during intermittent illumination. Biochim Biophys Acta 245:109–120CrossRefGoogle Scholar
  117. Jalink H, Van der Schoor R, Frandas A, Van Pijlen JG (1998) Chlorophyll fluorescence of Brassica oleracea seeds as a non-destructive marker for seed maturity and seed performance. Seed Sci Res 8:437–443CrossRefGoogle Scholar
  118. Joliot P, Kok B (1975) Oxygen evolution in photosynthesis. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, London, pp 387–411Google Scholar
  119. Jursinic P (1977) Photosystem II charge stabilization reactions in isolated chloroplasts. PhD Thesis, University of Illinois, Champaign, UrbanaGoogle Scholar
  120. Jursinic P (1986) Delayed fluorescence: current concepts and status. In: Amesz J, Fork DJ, Govindjee (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 291–328Google Scholar
  121. Jursinic P, Govindjee (1977) Temperature dependence of delayed light emission in the 6 to 340 microsecond range after a single flash in chloroplasts. Photochem Photobiol 26:617–628CrossRefGoogle Scholar
  122. Jursinic P, Govindjee, Wraight CA (1978) Membrane potential and microsecond to millisecond delayed light emission after a single excitation flash in isolated chloroplasts. Photochem Photobiol 27:61–71CrossRefGoogle Scholar
  123. Kalaji MH, Guo P (2008) Chlorophyll fluorescence: a useful tool in barley plant breeding programs. In: Sánchez A, Gutierrez SJ (eds) Photochemistry research progress. Nova Science Publishers, Inc., New York, pp 439–463Google Scholar
  124. Kalaji MH, Łoboda T (2007) Photosystem II of barley seedlings under cadmium and lead stress. Plant Soil Environ 53:511–516Google Scholar
  125. Kalaji MH, Nalborczyk E (1991) Gas exchange of barley seedlings growing under salinity stress. Photosynthetica 25:197–202Google Scholar
  126. Kalaji MH, Pietkiewicz S (1993) Salinity effects on plant growth and other physiological processes. Acta Physiol Plant 15:89–124Google Scholar
  127. Kalaji MH, Pietkiewicz S (2004) Some physiological indices to be exploited as a crucial tool in plant breeding. Plant Breed Seeds Sci 49:19–39Google Scholar
  128. Kalaji MH, Govindjee, Bosa K, Kościelniak J, Żuk-Gołaszewska K (2011a) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72CrossRefGoogle Scholar
  129. Kalaji MH, Bosa K, Kościelniak J, Hossain Z (2011b) Chlorophyll a fluorescence—a useful tool for the early detection of temperature stress in spring barley (Hordeum vulgare L.). OMICS 15:925–934PubMedCrossRefGoogle Scholar
  130. Kalaji MH, Carpentier R, Allakhverdiev SI, Bosa K (2012) Fluorescence parameters as an early indicator of light stress in barley. J Photochem Photobiol B 112:1–6PubMedCrossRefGoogle Scholar
  131. Kaňa R, Prášil O, Komárek O, Papageorgiou GC, Govindjee (2009) Spectral characteristic of fluorescence induction in a model cyanobacterium Synechococcus sp. (PCC 7942). Biochim Biophys Acta 1787:1170–1178PubMedCrossRefGoogle Scholar
  132. Kaňa R, Kotabová E, Komárek O, Šedivá B, Papageorgiou GC, Govindjee, Prášil O (2012) The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta 1817:1237–1247. doi:10.1016/j.bbabio.2012.02.024 PubMedCrossRefGoogle Scholar
  133. Katsumata M, Takeuchi A, Kazumura K, Koike T (2008) New feature of delayed luminescence: preillumination-induced concavity and convexity in delayed luminescence decay curve in the green alga Pseudokirchneriella subcapitata. J Photochem Photobiol B 90:152–162PubMedCrossRefGoogle Scholar
  134. Kautsky H, Hirsch A (1931) Neue Versuchezur Kohlensäureassimilation. Naturwissenschaften 19:964CrossRefGoogle Scholar
  135. Klimov VV, Allakhverdiev SI, Pashchenko VZ (1978) Measurement of the activation energy and life-time of the fluorescence of photosystem 2 chlorophyll. Dokl Acad Nauk SSSR 242:1204–1207Google Scholar
  136. Klughammer C, Schreiber U (1998) Measuring P700 absorbance changes in the near infrared spectral region with a dual wavelength pulsemodulation system. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers, Dordrecht, pp 4357–4360Google Scholar
  137. Klughammer C, Kolbowski J, Schreiber U (1990) LED array spectrophotometer for measurement of time-resolved difference spectra in the 530–600 nm wavelength region. Photosynth Res 25:317–327CrossRefGoogle Scholar
  138. Kocsis P, Asztalos E, Gingl Z, Maróti P (2010) Kinetic bacteriochlorophyll fluorometer. Photosynth Res 105:73–82PubMedCrossRefGoogle Scholar
  139. Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106PubMedCrossRefGoogle Scholar
  140. Kolber Z, Klimov D, Ananyev G, Rascher U, Berry J, Osmond B (2005) Measuring photosynthetic parameters at a distance: laser induced fluorescence transient (LIFT) method for remote measurements of photosynthesis in terrestrial vegetation. Photosynth Res 84:121–129PubMedCrossRefGoogle Scholar
  141. Kolbowski J, Reising H, Schreiber U (1990) Computer controlled pulse modulation system for analysis of photo-acoustic signals in the time domain. Photosynth Res 25:309–316CrossRefGoogle Scholar
  142. Konstantinova P, Van der Schoor R, Van den Bulk RW, Jalink H (2002) Chlorophyll fluorescence sorting as a method for improvement of barley (Hordeum vulgare L.) seed health and germination. Seed Sci Technol 30:411–421Google Scholar
  143. Kościelniak J, Ostrowska A, Biesaga-Kościelniak J, Filek W, Janeczko A, Kalaji MH, Stalmach K (2011) The effect of zearalenone on PSII photochemical activity and growth in wheat and soybean under salt (NaCl) stress. Acta Physiol Plant 33:2329–2338CrossRefGoogle Scholar
  144. Kramer DM, Howard R, Robinson HR, Antony R, Crofts AR (1990) A portable multi-flash kinetic fluorometer for measurement of donor and acceptor reactions of photosystem 2 in leaves of intact plants under field conditions. Photosynth Res 26:181–193CrossRefGoogle Scholar
  145. Krasnovsky AA Jr (1982) Delayed fluorescence and phosphorescence of plant pigments. Photochem Photobiol 36:733–741CrossRefGoogle Scholar
  146. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349CrossRefGoogle Scholar
  147. Krause GH, Vernotte C, Briantais JM (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. Biochim Biophys Acta 679:116–124CrossRefGoogle Scholar
  148. Krey A, Govindjee (1963) Fluorescence change in Porphyridium exposed to green light of different intensity: a new emission band at 693 nm and its significance to photosynthesis. Proc Natl Acad Sci USA 52:1568–1572CrossRefGoogle Scholar
  149. Küpper H, Andresen E, Wiegert S, Šimek M, Leitenmaier B, Šetlík I (2009) Reversible coupling of individual phycobiliprotein isoforms during state transitions in the cyanobacterium Trichodesmium analysed by single-cell fluorescence kinetic measurements. Biochim Biophys Acta 1787:155–167PubMedCrossRefGoogle Scholar
  150. Lakowicz JR (1983) Principles of fluorescence spectroscopy. Plenum Press, New YorkCrossRefGoogle Scholar
  151. Lakowicz JR (1999) Principles of fluorescence spectroscopy, 2nd edn. Kluwer Academic (now Springer), New YorkGoogle Scholar
  152. Lang M, Lichtenthaler HK (1991) Changes in the blue-green and red fluorescence emission spectra of beech leaves during the autumnal chlorophyll breakdown. J Plant Physiol 138:550–553CrossRefGoogle Scholar
  153. Lavorel J (1959) Induction of fluorescence in quinone poisoned Chlorella cells. Plant Physiol 34:204–209PubMedCrossRefGoogle Scholar
  154. Lavorel J (1963) Hétérogénéité de la chlorophylle in vivo I Spectresd’émission de fluorescence. Biochim Biophys Acta 60:510–523CrossRefGoogle Scholar
  155. Lavorel J (1969) On the relation between fluorescence and luminescence in photosynthetic systems. In: Metzner H (ed) Progress in Pphotosynthesis research, vol 2. International Union of Biological Science, Tübingen, pp 883–898Google Scholar
  156. Lavorel J (1975) Luminescence. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 223–317Google Scholar
  157. Lawlor D (2001) Photosynthesis, 3rd edn. Springer, BerlinGoogle Scholar
  158. Lazar D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1–28PubMedCrossRefGoogle Scholar
  159. Lejealle S, Evain S, Cerovic ZG (2010) Multiplex: a new diagnostic tool for management of nitrogen fertilization of turfgrass. 10th International conference on precision agriculture, Denver, Colorado, 18–21 July 2010, CD-ROM 15Google Scholar
  160. Lichtenthaler HK, Rinderle U (1988) The role of fluorescence in the detection of stress conditions in plants. CRC Crit Rev Anal Chem 12(Supplement 1):29–85Google Scholar
  161. Logan BA, Adams WW III, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis in the field. Funct Plant Biol 34:853–859CrossRefGoogle Scholar
  162. Loria S (1925) Indirectly excited fluorescence spectra. Phys Rev 26:573–584CrossRefGoogle Scholar
  163. Lurie S, Cohen W, Bertsch W (1972) Delayed light studies in photosynthetic energy conversion. V. millisecond emission from digitonin sub-chloroplast fractions. In: Forti G, Avron M, Melandri A (eds) Proceedings of the 2nd international congress of photosynthesis research, vol I. Dr. W. Junk N.V. Publishers, The Hague, pp 197–205Google Scholar
  164. MacAlister ED, Myers J (1940) The time course of photosynthesis and fluorescence observed simultaneously. Smithson Misc Collect 99:1–37Google Scholar
  165. Malkin S (1977) Delayed luminescence. In: Barber J (ed) Primary processes in photosynthesis. Elsevier, Amsterdam, pp 349–430Google Scholar
  166. Malkin S (1979) Delayed luminescence. In: Avron M, Trebst A (eds) Photosynthesis I. Photosynthetic electron transport and photophosphorylation . Academic Press, New York, pp 473–491Google Scholar
  167. Malkin S, Barber J (1978) Induction patterns of delayed luminescence from isolated chloroplasts. I. Response of delayed luminescence to changes in the prompt fluorescence yield. Biochim Biophys Acta 502:524–541PubMedCrossRefGoogle Scholar
  168. Malkin S, Bilger W, Schreiber U (1994) The relationship between luminescence and fluorescence in tobacco leaves during the induction period. Photosynth Res 39:57–66CrossRefGoogle Scholar
  169. Mar T, Govindjee (1971) Thermoluminescence in spinach chloroplast and in Chlorella. Biochim Biophys Acta 226:200–203PubMedCrossRefGoogle Scholar
  170. Mar T, Roy G (1974) A kinetic model of the primary back reaction in photosynthesis of green plants. J Theor Biol 48:257–281PubMedCrossRefGoogle Scholar
  171. Mar T, Brebner J, Roy G (1975) Induction kinetics of delayed light emission in spinach chloroplasts. Biochim Biophys Acta 376:345–353PubMedCrossRefGoogle Scholar
  172. Matorin DN, Venediktov PS, Gashimov RM, Rubin AB (1976) Millisecond delayed fluorescence activated by reduced DPIP in DCMU-treated chloroplasts and in subchloroplast particles. Photosynthetica 10:266–273Google Scholar
  173. Matorin DN, Marenkov VS, Dobrynin SA, Ortoidze TV, Venediktov PS (1978) Device for recording of delayed fluorescence in photosynthetic organisms with pulse illumination mode. Nauch Dokl Vyshey Scholy, Ser Biol Nauki (Moskow) 11:127–132 (in Russian)Google Scholar
  174. Matsubara S, Chen Y-C, Caliandro R, Govindjee, Clegg RM (2011) Photosystem II fluorescence lifetime imaging in avocado leaves: contributions of the lutein-epoxide and violaxanthin cycles to fluorescence quenching. J Photochem Photobiol B 104:271–284PubMedCrossRefGoogle Scholar
  175. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  176. Merz D, Geyer M, Moss DA, Ache HJ (1996) Chlorophyll fluorescence biosensor for the detection of herbicides. Fresen J Anal Chem 354:299–305Google Scholar
  177. Mi H, Klughammer C, Schreiber U (2000) Light-induced dynamic changes of NADPH fluorescence in Synechocystis PCC 6803 and its ndhB-defective Mutant M55. Plant Cell Physiol 41:1129–1135PubMedCrossRefGoogle Scholar
  178. Miloslavina Y, Szczepaniak M, Müller M, Sander J, Nowaczyk M, Rögner M, Holzwarth AR (2006) Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study. Biochemistry 45:2436–2442PubMedCrossRefGoogle Scholar
  179. Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta 1767:327–334PubMedCrossRefGoogle Scholar
  180. Mohanty P, Papageorgiou GC, Govindjee (1971) Fluorescence induction in the red alga Porphyridium cruentum. Photochem Photobiol 14:667–682CrossRefGoogle Scholar
  181. Moss RA, Loomis WE (1952) Absorption spectra of leaves. I The visible spectrum. Plant Physiol J 27:370–391CrossRefGoogle Scholar
  182. Moya I, Camenen L, Evain S, Goulas Y, Cerovic ZG, Latouche G, Flexas J, Ounis A (2004) A new instrument for passive remote sensing. 1. Measurements of sunlight-induced chlorophyll fluorescence. Remote Sens Environ 91:186–197CrossRefGoogle Scholar
  183. Müller NJC (1874) Beziehungenzwischen Assimilation, Absorption und Fluoreszenzim Chlorophyll des lebenden Blattes. Jahrb Wiss Bot 9:42–49Google Scholar
  184. Munday JCM Jr, Govindjee (1969a) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:1–21PubMedCrossRefGoogle Scholar
  185. Munday JCM Jr, Govindjee (1969b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. IV. The effect of pre-illumination on the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:22–35PubMedCrossRefGoogle Scholar
  186. Murkowski A (2002) Oddziaływanie czynników stresowych na luminescencję chlorofilu w aparacie fotosyntetycznym roślin uprawnych. (Effects of some stress factors on chlorophyll luminescence in the photosynthetic apparatus crop plants) [Monograph in Polish]. Acta Agroph 61:6–158Google Scholar
  187. Murkowski A, Prokowski Z (2003) Zastosowanie metody luminescencyjnej do oznaczania chlorofilu a w fitoplanktonie [in Polish]. Acta Agroph 93:43–54Google Scholar
  188. Nedbal L, Soukupová J, Whitmarsh J, Trtílek M (2000a) Postharvest imaging of chlorophyll fluorescence from lemons can be used to predict fruit quality. Photosynthetica 38:571–579CrossRefGoogle Scholar
  189. Nedbal L, Soukupová J, Kaftan D, Whitmarsh J, Trtílek M (2000b) Kinetic imaging of chlorophyll fluorescence using modulated light. Photosynth Res 66:3–12PubMedCrossRefGoogle Scholar
  190. Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination. I. Saturation characteristics and partial control by the photosystem II acceptor side. Z Naturforsch 42:1246–1254Google Scholar
  191. Neverov K, Santabarbara S, Krasnovsky A (2011) Phosphorescence study of chlorophyll d photophysics. Determination of the energy and lifetime of the photo-excited triplet state. Evidence of singlet oxygen photosensitization. Photosynth Res 108:101–106PubMedCrossRefGoogle Scholar
  192. Noomnarm U, Clegg RM (2009) Fluorescence lifetimes: fundamentals and interpretations. Photosynth Res 101:181–191PubMedCrossRefGoogle Scholar
  193. Ögren E, Baker NR (1985) Evaluation of a technique for the measurement of chlorophyll fluorescence from leaves exposed to continuous white light: technical report. Plant Cell Environ 8:539–548CrossRefGoogle Scholar
  194. Papageorgiou GC, Govindjee (1968a) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. II. Chorella pyrenoidosa. Biophys J 8:1316–1328PubMedCrossRefGoogle Scholar
  195. Papageorgiou GC, Govindjee (1968b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. I. Anacystis nidulans. Biophys J 8:1299–1315PubMedCrossRefGoogle Scholar
  196. Papageorgiou GC, Govindjee (2004, reprinted 2010) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, DordrechtGoogle Scholar
  197. Papageorgiou GC, Govindjee (2011) Photosystem II fluorescence: slow changes—scaling from the past. J Photochem Photobiol B 104:258–270PubMedCrossRefGoogle Scholar
  198. Pelletier J, Caventou JB (1818) Notice sur la matiltreverte des feuilles [chlorophylle]. Ann Chim Phys IX:194–196Google Scholar
  199. Porcar-Castell A (2008) Studying the diurnal and seasonal acclimation of photosystem II using chlorophyll a fluorescence. PhD thesis, Dissertationes Forestales 69, University of HelsinkiGoogle Scholar
  200. Prasad A, Pospíšil P (2011) Linoleic acid-induced ultra-weak photon emission from Chlamydomonas reinhardtii as a tool for monitoring of lipid peroxidation in the cell membranes. PLoS One 6(7):e22345. doi:10.1371/journal.pone.0022345 PubMedCrossRefGoogle Scholar
  201. Quick WP, Horton P (1984) Studies on the induction of chlorophyll fluorescence in barley protoplasts. I. Factors affecting the observation of oscillations in the yield of chlorophyll fluorescence and the rate of oxygen evolution. Proc R Soc Lond 220:361–370CrossRefGoogle Scholar
  202. Rabinowitch E (1951) Photosynthesis and related processes, vol 11. Part 1, Spectroscopy and fluorescence of photosynthetic pigments; kinetics of photosynthesis. Wiley, New YorkGoogle Scholar
  203. Radenovic C, Markovic D, Jeremic M (1994) Delayed chlorophyll fluorescence in plant models. Photosynthetica 30:1–24Google Scholar
  204. Rajagopal S, Bukhov NG, Carpentier R (2003) Photoinhibitory light-induced changes in the composition of chlorophyll–protein complexes and photochemical activity in photosystem I submembrane fractions. Photochem Photobiol 77:284–291PubMedCrossRefGoogle Scholar
  205. Reising H, Schreiber U (1992) Pulse-modulated photoacoustic measurements reveal strong gas-uptake component at high CO2 concentrations. Photosynth Res 31:227–238CrossRefGoogle Scholar
  206. Romanowska-Duda B, Kalaji MH, Strasser RJ (2005) The use of PSII activity of Spirodela oligorrhiza plants as an indicator for water toxicity. In: Van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects to global perspectives. Allen Press, Lawrence, pp 585–587Google Scholar
  207. Romanowska-Duda ZB, Grzesik M, Kalaji MH (2010) Physiological activity of energy plants fertilized with sevage sludge and usefulness of the Phytotoxkit test in practice. Environ Protect Eng 36:73–81Google Scholar
  208. Romero E, Diner BA, Nixon PJ, Coleman WJ, Dekker JP, van Grondelle R (2012) Mixed exciton–charge-transfer states in photosystem II: stark spectroscopy on site-directed mutants. Biophys J 103:185–194PubMedCrossRefGoogle Scholar
  209. Rutherford AW, Inoue Y (1984) Oscillation of delayed luminescence from PSII: recombination of S2QB- and S3QB-. FEBS Lett 165:163–170CrossRefGoogle Scholar
  210. Rutherford AW, Govindjee, Inoue Y (1984) Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proc Natl Acad Sci USA 81:1107–1111PubMedCrossRefGoogle Scholar
  211. Satoh K, Katoh S (1983) Induction kinetics of millisecond-delayed luminescence in intact Bryopsis chloroplasts. Plant Cell Physiol 24:953–962CrossRefGoogle Scholar
  212. Satoh K, Strasser RJ, Butler WL (1976) A demonstration of energy transfer from photosystem II to photosystem I in chloroplasts. Biochim Biophys Acta 440:337–345PubMedCrossRefGoogle Scholar
  213. Schansker G, Srivastava A, Govindjee, Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30:785–796CrossRefGoogle Scholar
  214. Schatz GH, Brock H, Holzwarth AR (1988) Kinetic and energetic model for the primary processes in photosystem II. Biophys J 54:397–405PubMedCrossRefGoogle Scholar
  215. Schreiber U (1998) Chlorophyll fluorescence: new instruments for special applications. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers (now Springer), Dordrecht, pp 4253–4258Google Scholar
  216. Schreiber U (2004) Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overwiev. In: Papageorgiu GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 279–319Google Scholar
  217. Schreiber U, Krieger A (1996) Hypothesis: two fundamentally different types of variable fluorescence in vivo. FEBS Lett 397:131–135PubMedCrossRefGoogle Scholar
  218. Schreiber U, Neubauer C (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination. II. Partial control by the photosystem I1 donor side and possible ways of interpretation. Z Naturforsch 42:1255–1264Google Scholar
  219. Schreiber U, Schliwa U (1987) A solid-state, portable instrument for measurement of chlorophyll luminescence induction in plants. Photosynth Res 11:173–182CrossRefGoogle Scholar
  220. Schreiber U, Groberman L, Vidaver W (1975) Portable, solid state fluorometer for the measurement of chlorophyll fluorescence induction in plants. Rev Sci Instrum 46:538–542CrossRefGoogle Scholar
  221. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical fluorescence quenching with a new type of modulation fluorimeter. Photosynth Res 10:51–62CrossRefGoogle Scholar
  222. Schreiber U, Klughammer C, Kolbowski J (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photosynth Res. doi:10.1007/s11120-012-9758-1 PubMedGoogle Scholar
  223. Seppälä J, Tamminen T, Kaitala S (1999) Experimental evaluation of nutrient limitation of phytoplankton communities in the Gulf of Riga. J Mar Syst 23:107–126CrossRefGoogle Scholar
  224. Shelaev IV, Gostev FE, Vishnev MI, Shkuropatov AY, Ptushenko VV, Mamedov MD, Sarkisov OM, Nadtochenko VA, Semenov AY, Shuvalov VA (2011) P680 (P(D1)P(D2)) and Chl(D1) as alternative electron donors in photosystem II core complexes and isolated reaction centers. J Photochem Photobiol B 104(1–2):44–50PubMedCrossRefGoogle Scholar
  225. Shimony C, Spencer J, Govindjee (1967) Spectral characterestics of Anacystis particles. Photosynthetica 1:113–125Google Scholar
  226. Shinkarev VP, Xu C, Govindjee, Wraight CA (1997) Kinetics of the oxygen evolution step in plants determined from flash-induced chlorophyll a fluorescence. Photosynth Res 51:43–49CrossRefGoogle Scholar
  227. Shuvalov VA (1976) The study of the primary photoprocess in photosystem I of chloroplasts: recombination luminescence, chlorophyll triplet state and triplet–triplet annihilation. Biochim Biophs Acta 430:113–121CrossRefGoogle Scholar
  228. Sonneveld A, Duysens LNM, Moerdijk A (1980a) Magnetic field-induced increase in chlorophyll a delayed fluorescence of photosystem II: a 100- to 200-ns component between 4.2 and 300 K. Proc Natl Acad Sci USA 77:5889–5893PubMedCrossRefGoogle Scholar
  229. Sonneveld A, Rademaker H, Duysens LNM (1980b) Microsecond delayed fluorescence of photosystem II of photosynthesis in various algae: emission spectra and uphill energy transfer. FEBS Lett 113:323–327CrossRefGoogle Scholar
  230. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications. J Photochem Photobiol B104:236–257Google Scholar
  231. Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise. Photosynth Res. doi:10.1007/s11120-012-9754-5 PubMedGoogle Scholar
  232. Stokes GG (1852) On the change of refrangibility of light. Philos Trans R Soc Lond 142:463–562CrossRefGoogle Scholar
  233. Strasser RJ (1973a) Das simultane Erfassen von polarographischen, absorptions- und fluoreszenzspektroskopischen: messungen zur Lokalisierung von photosynthetischen Regulationsmechanismen. Verh Schweiz Nat Ges 73:82–86Google Scholar
  234. Strasser RJ (1973b) Induction phenomena in green plants when the photosynthetic apparatus starts to work. Arch Int Physiol Biochim 81:935–955PubMedCrossRefGoogle Scholar
  235. Strasser RJ (1974) A new device for simlultaneous measurements of oxygen concentration, absorption and fluorescence changes in photosynthetic systems. Experientia 30:320PubMedCrossRefGoogle Scholar
  236. Strasser RJ (1978) The grouping model of plant photosynthesis. In: Akoyunoglou G, Argyroudi-Akoyunoglou JH (eds) Chloroplast development. Elsevier/North Holland Biomedical Press, Amsterdam, pp 514–524Google Scholar
  237. Strasser RJ (1985) Dissipative Struktguren als Thermodynamischer Regelkreis des Photosyntheseapparates. Ber Deutsch Bot Ges Bd 98:53–72Google Scholar
  238. Strasser RJ (1986) Laser-induced fluorescence of plants and its application in environmental research. In: Proceedings of IGARSS 86 symposium, ESA Publications Division, Zürich, pp 1581–1585Google Scholar
  239. Strasser B J, Strasser R J (1995) Measuring fast fluorescence transients to address environmental questions: The JIP test. In: Mathis (ed) Photosynthesis: from light to biosphere, vol V. Proceedings of the Xth international photosynthesis congress, Montpellier, France. Kluwer Academic Publishers (now Springer), Dordrecht, pp. 977–980Google Scholar
  240. Strasser RJ, Butler WL (1977a) Energy transfer and the distribution of excitation energy in the photosynthetic apparatus of spinach chloroplasts. Biochim Biophys Acta 460:230–238PubMedCrossRefGoogle Scholar
  241. Strasser RJ, Butler WL (1977b) The yield of energy transfer and the spectral distribution of excitation energy in the photochemical apparatus of flashed bean leaves. Biochim Biophys Acta 462:295–306PubMedCrossRefGoogle Scholar
  242. Strasser RJ, Govindjee (1992) On the O–J–I–P fluorescence transients in leaves and D1 mutants of Chlamydomonas reinhardtii. In: Murata N (ed) Research in photosynthesis, vol 11. Kluwer Academic, Dordrecht, pp 29–32Google Scholar
  243. Strasser RJ, Sironval C (1973) Induction of PSII activity and induction of a variable part of the fluorescence emission by weak green light in flashed bean leaves. FEBS Lett 29:286–288PubMedCrossRefGoogle Scholar
  244. Strasser RJ, Sironval C (1974) Correlation between the induction of oxygen evolution and of variable fluorescence in flashed bean leaves. Plant Sci Lett 3:135–140CrossRefGoogle Scholar
  245. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42CrossRefGoogle Scholar
  246. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004, reprinted 2010) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 321–362Google Scholar
  247. Strasser RJ, Tsimilli-Michael M, Dangre D, Rai M (2007) Biophysical phenomics reveals functional building blocks of plants systems biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora indica. In: Varma A, Oelmüller R (eds) Advanced techniques in soil microbiology. Soil biology, vol 11. Springer, HeidelbergGoogle Scholar
  248. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797(2010):1313–1326PubMedGoogle Scholar
  249. Strehler B (1951) The luminescence of isolated chloroplasts. Arch Bitch Biophys 34:239–248CrossRefGoogle Scholar
  250. Strehler B (1996) Halcyon days with Bill Arnold. Photosynth Res 48:11–18CrossRefGoogle Scholar
  251. Strehler BL, Arnold W (1951) Light production by green plants. J Gen Physiol 34:809–820PubMedCrossRefGoogle Scholar
  252. Sweeney BM, Prezelin BB, Wong D, Govindjee (1979) In vivo chlorophyll a fluorescence transients and the circadian rhythm of photosynthesis in Gonyaulax polyedra. Photochem Photobiol 30:309–311PubMedCrossRefGoogle Scholar
  253. Swoczyna T, Kalaji MH, Pietkiewicz S, Borowski J, Zaraś-Januszkiewicz E (2010a) Photosynthetic apparatus efficiency of eight tree taxa as an indicator of their tolerance to urban environments. Dendrobiology 63:65–75Google Scholar
  254. Swoczyna T, Kalaji MH, Pietkiewicz S, Borowski J, Zaraś-Januszkiewicz E (2010b) Monitoring young urban trees tolerance to roadside conditions by application of chlorophyll fluorescence technique. Zesz Probl Post N Rol 545:303–309Google Scholar
  255. Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of stress impact on plant’s vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: genetics and molecular biology, eco-function, biotechnology, eco-physiology, and structure and systematics. Springer, Berlin, pp 679–703Google Scholar
  256. Tuba Z, Saxena DK, Srivastava K, Singh S, Sz Czebol, Kalaji MH (2010) Chlorophyll a fluorescence measurements for validating the tolerant bryophytes for heavy metal (Pb) biomapping. Curr Sci 98:1505–1508Google Scholar
  257. Turzó K, Laczkó G, Maróti P (1998) Delayed fluorescence study on P*QA → P + QA charge separation energetics linked to protons and salt in reaction centers from Rhodobacter sphaeroides. Photosynth Res 55:235–240CrossRefGoogle Scholar
  258. Valeur B (2001) Molecular fluorescence. Principles and applications. Wiley, WeinheimCrossRefGoogle Scholar
  259. Valeur B, Berberan-Santos MN (2012) Molecular fluorescence: principles and applications, 2nd edn. Wiley, WeinheimCrossRefGoogle Scholar
  260. Valeur B, Brocon J-C (2001) New trends in fluorescence spectroscopy: applications to chemical and life sciences. Springer, New YorkGoogle Scholar
  261. Van Rensen JJS, Vredenberg WJ, Rodrigues GC (2007) Time sequence of the damage to the acceptor and donor sides of photosystem II by UV-B radiation as evaluated by chlorophyll a fluorescence. Photosynth Res 94:291–297PubMedCrossRefGoogle Scholar
  262. Venediktov PS, Matorin DN, Rubin AB (1969) Izuchenie zavisimosti poslevecheniyafotosinteziruyushchikh organizmov ot intensivnosti vozozhdayushchego sveta. (Dependence of after-glow of photosynthetyzing organism on the exciting irradiance). Nauch Dokl vyssh Shkoly, boil Nauki 12(2):46–51Google Scholar
  263. Vernon LP, Klein S, White FG, Shaw ER, Mayne BC (1972) Properties of a small photosystem II particle obtained from spinach chloroplasts. In: Forti G, Avron M, Melandri A (eds) Proceedings of the 2nd international congress of photosynthesis research, vol I. Dr. W. Junk N.V. Publishers, The Hague, pp 801–812Google Scholar
  264. Veselovskii V, Veselova T (1990) Plant luminescence: theoretical and practical aspects [in Russian]. Nauka, MoscowGoogle Scholar
  265. Vredenberg WJ, Van Rensen JJS, Rodrigues GC (2006) On the sub-maximal yield and photo-electric stimulation of chlorophyll a fluorescence in single turnover excitations in plant cells. Bioelectrochemistry 68:81–88PubMedCrossRefGoogle Scholar
  266. Walker DA (1981) Secondary fluorescence kinetics of spinach leaves in relation to the onset of photosynthetic carbon metabolism. Planta 153:273–278CrossRefGoogle Scholar
  267. Walker DA (1987) The use of the oxygen electrode and fluorescence probes in simple measurements of photosynthesis. Oxygraphics Limited, Sheffield, pp 1–145Google Scholar
  268. Walker DA, Osmond CB (1986) Measurement of photosynthesis in vivo with a leaf disc electrode: correlations between light dependence of steady state photosynthetic O2 evolution and chlorophyll a fluorescence transients. Proc R Soc Lond B 227:267–280CrossRefGoogle Scholar
  269. Walker DA, Sivak MN, Prinsley RT, Cheesbrough JK (1983) Simultaneous measurement of oscillations in oxygen evolution and chlorophyll a fluorescence in leaf pieces. Plant Physiol 73:542–549PubMedCrossRefGoogle Scholar
  270. Warburg O (1920) Über die Geschwindigkeit der Photochemischen Kohlensäurezeresetzung in Lebenden Zellen II. Biochem Z 103:188–217Google Scholar
  271. Wong D, Govindjee, Jursinic P (1978) Analysis of microsecond fluorescence yield and delayed light emission changes after a single flash in pea chloroplasts: effects of mono-and divalent cations. Photochem Photobiol 28:963–974CrossRefGoogle Scholar
  272. Wraight CA, Crofts AT (1971) Delayed fluorescence and the high-energy state of chloroplasts. Eur J Biochem 19:386–397PubMedCrossRefGoogle Scholar
  273. Yamagishi A, Satoh K, Katoh S (1978) Fluorescence induction in chloroplasts isolated from the green alga Bryopsis maxima. III. A fluorescence transient indicating proton gradient across the thylakoid membrane. Plant Cell Physiol 19:17–25Google Scholar
  274. Yordanov I, Goltsev V, Stoyanova T, Venediktov P (1987) High temperature damage and acclimation of the photosynthetic apparatus. I. Temperature sensitivity of some photosynthetic parameters of chloroplasts isolated from acclimated and non-acclimated bean leaves. Planta 170:471–477CrossRefGoogle Scholar
  275. Yordanov I, Goltsev V, Stefanov D, Chernev P, Zaharieva I, Kirova M, Gecheva V, Strasser RJ (2008) Preservation of PS II electron transport from senescence-induced inactivation in primary leaves after decapitation and defoliation of bean plants. J Plant Physiol 165:1954–1963PubMedCrossRefGoogle Scholar
  276. Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee, Sarin NM (2010) Overexpression of y-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll fluorescence measurements. Biochim Biophys Acta 1791:428–438Google Scholar
  277. Zaharieva I, Goltsev V (2003) Advances on photosystem II investigation by measurement of delayed chlorophyll fluorescence by a phosphoroscopic method. Photochem Photobiol 77:292–298PubMedCrossRefGoogle Scholar
  278. Zaharieva I, Taneva SG, Goltsev V (2001) Effect of temperature on the luminescent characteristics in leaves of Arabidopsis mutants with decreased unsaturation of the membrane lipids. Bulg J Plant Physiol 27:3–18Google Scholar
  279. Zaharieva I, Wichmann J, Dau H (2011) Thermodynamic limitations of photosynthetic water oxidation at high proton concentrations. J Biol Chem 286:1822–1828CrossRefGoogle Scholar
  280. Živčák M, Olšovská K, Brestič M, Slabbert MM (2010) Critical temperature derived from the selected chlorophyll a fluorescence parameters of indigenous vegetable species of South Africa treated with high temperature. In: Photosynthesis research for food fuel and the future: 15th international congress of photosynthesis, 22–27 August 2010, Beijing, pp 281–282Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Hazem M. Kalaji
    • 1
  • Vasilij Goltsev
    • 2
  • Karolina Bosa
    • 3
  • Suleyman I. Allakhverdiev
    • 4
    • 5
  • Reto J. Strasser
    • 6
    • 7
    • 8
  • Govindjee
    • 9
  1. 1.Department of Plant PhysiologyFaculty of Agriculture and Biology, Warsaw University of Life Sciences SGGWWarsawPoland
  2. 2.Department of Biophysics and RadiobiologyFaculty of Biology St. Kliment Ohridski University of SofiaSofiaBulgaria
  3. 3.Department of PomologyFaculty of Horticulture and Landscape Architecture, Warsaw University of Life Sciences SGGWWarsawPoland
  4. 4.Institute of Plant Physiology, Russian Academy of SciencesMoscowRussia
  5. 5.Institute of Basic Biological Problems, Russian Academy of SciencesPushchinoRussia
  6. 6.Bioenergetics LaboratoryUniversity of GenevaJussy, GenevaSwitzerland
  7. 7.Weed Research LaboratoryNanjing Agricultural UniversityNanjingChina
  8. 8.Research Unit Environmental Science and ManagementNorth-West University (Potchefstroom Campus)PotchefstroomRepublic of South Africa
  9. 9.Department of Biochemistry, Department of Plant Biology, and Center of Biophysics & Computational BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

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